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Revisiting Telegony: Offspring Inherit An Acquired Characteristic of Their Mother's Previous Mate
Revisiting Telegony: Offspring Inherit An Acquired Characteristic of Their Mother's Previous Mate
12373
Abstract
Angela J. Crean,* Anna M. Kopps†, Newly discovered non-genetic mechanisms break the link between genes and inheritance, thereby
and Russell Bonduriansky also raising the possibility that previous mating partners could influence traits in offspring sired
by subsequent males that mate with the same female (‘telegony’). In the fly Telostylinus angusticol-
Evolution and Ecology Research
lis, males transmit their environmentally acquired condition via paternal effects on offspring body
Centre and School of Biological,
size. We manipulated male condition, and mated females to two males in high or low condition in
Earth and Environmental Sciences
a fully crossed design. Although the second male sired a large majority of offspring, offspring
University of New South Wales
Sydney, NSW, 2052, Australia
body size was influenced by the condition of the first male. This effect was not observed when
females were exposed to the first male without mating, implicating semen-mediated effects rather
†
Present address: Marine Evolution
than female differential allocation based on pre-mating assessment of male quality. Our results
and Conservation, Centre for reveal a novel type of transgenerational effect with potential implications for the evolution of
Ecological and Evolutionary Studies reproductive strategies.
University of Groningen,
Nijenborgh 7, 9747 AG Groningen, Keywords
The Netherlands Condition, diet, inheritance of acquired traits, non-genetic inheritance, paternal effect, plasticity,
seminal proteins, telegony.
*Correspondence:
E-mail: a.crean@unsw.edu.au
Ecology Letters (2014) 17: 1545–1552
(a)
Initial mating (first male) 1st condition 2nd condition
while ovules are
immature High High
or or
Low Low
Offspring
1 week old 3 weeks old
Ovule development (Ovules immature) (Ovules mature)
(b)
Housing treatment 2nd
Mating or
Subsequent mating
(second male) when eggs
are mature (chorionated), No-mating or
resulting in fertilization
Partition or
© 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.
Letter Telegonic effects of male condition 1547
larval diet were significantly larger than males raised on a and Image J was used to measure thorax length as an index
poor larval diet (male thorax length mean SE: of body size.
rich = 2.552 0.046 mm, poor = 1.726 0.017 mm; t100 =
17.111, P < 0.001).
Paternity analysis
Larval containers were kept in a controlled-environment
chamber set to an alternating light–dark 12–12 h cycle of 25/ All parental generation males and females were frozen imme-
23°C and 50% humidity, and periodically misted with water. diately after mating/oviposition and their thorax lengths later
Upon eclosion, flies were separated by sex and larval diet measured as described above. DNA was extracted from the
treatment, and housed with ad libitum food (brown sugar and parents and a subsample of five offspring per family where
yeast) and water: poor females were discarded; rich females possible (Table S1) from high–low and low–high treatment
were housed individually in 250 mL containers; rich and poor groups. DNA was extracted with a Gentra PureGene DNA
males were housed in groups of 10 individuals in 2 L contain- extraction kit (Qiagen), and six microsatellite markers (Tangus
ers. Of females used as mothers in the experiment (n = 26 per 2, 8, 9, 10, 15, 20 (see Kopps et al. 2013); Table S2) were
treatment combination), two died before the second mating amplified as described in Kopps et al. (2013), run on an ABI
(one low-high, one high-high treatment) and were excluded 3730 DNA Analyser, and analysed with GeneMapper ver. 3.7
from analysis. Female body size did not differ among treat- software (both Applied Biosystems, Foster City, CA, USA).
ment groups (F2,101 = 0.702; P = 0.498). No treatment males We successfully genotyped 205 individual offspring, their 48
died during the experiment. mothers and probable sires (second males), and 30 of 51 alter-
native potential first males (males from low–low and high–
high treatments). Individuals were excluded from the data set
Telegony experiment
if less than four microsatellite loci amplified successfully (25
Seven days after eclosion (while their ovules were still imma- offspring and 26 potential sires), or if offspring had any mis-
ture), females were paired with either a high-condition (rich matches with their mother (7 individuals). The individual
larval diet) or low-condition (poor larval diet) male, and left identity of the second male was known, and the genotypes of
to mate for 24 h. The males were then returned to their group most potential alternative sires were present in the data set.
cages and females left to mature in their individual cages. Hence, we assessed paternity for the putative sire (second
Females do not lay eggs unless given appropriate oviposition male) and potential alternative sires (first males) by non-exclu-
media, and therefore did not lay any eggs during this time. sion (i.e. zero mismatching alleles with the second male after
Two weeks after the initial mating (when their ovules were the maternal contribution was accounted for, see Supporting
mature), females were paired to a second male for 24 h in a Information for further details) using the output table in Cer-
fully crossed design, resulting in four combinations of first vus (Marshall et al. 1998).
and second male condition (high–high, high–low, low–high,
low–low), and given oviposition medium to lay eggs (Fig. 2a).
Female differential allocation experiment
To avoid cohort effects, the second male was drawn from the
same set of males that had been used for the first mating, such To determine whether the effect of the first male’s condition
that each male was used both as a first male and as a second on offspring body size was mediated by semen-borne factors
male. We allowed 2 weeks between the first and second mat- or by female differential allocation based on pre-mating
ings to allow females’ ovules to mature and minimise the assessment of male quality, we performed a separate experi-
prevalence of viable sperm from the first mating in female ment in which females were either mated to the first male
sperm-storage organs. Twenty randomly chosen eggs from (mating treatment), allowed to interact but not mate with the
each female were transferred into a container with 100 mL of first male (no-mating treatment), or housed adjacent to the
poor larval medium. A subsample of eggs from each female first male with a mesh partition between the male and female
(mean n = 9.08, SD = 2.30, Table S1) was also photographed (partition treatment) (Fig. 2b). The mating treatment allowed
under a Leica MS5 stereoscope (Leica Microsystems, Wetzlar, semen transfer by both males (as in the telegony experiment),
Germany) fitted with a Leica DFC420 camera, and egg area whereas the no-mating treatment prevented ejaculate transfer
was measured from images using Image J software (National by the first male, thus allowing us to test for differential allo-
Institutes of Health, Bethesda, Maryland, USA). cation based on pre-mating assessment. The partition treat-
Larvae were left to develop in a controlled-environment ment was intended to establish whether male chemosensory
chamber, as described above. Adult flies (offspring) were and (limited) visual cues were sufficient to allow for female
allowed to emerge into 2 L cages, with food and water pro- assessment of male condition and differential allocation (if
vided ad libitum. The date of first emergence was recorded for any).
each family (replicate), and after 10 days (when flies had In the mating treatment, week-old females were allowed to
ceased emerging) all adult offspring were counted and frozen mate with a male in either high or low condition (nhigh = 18,
(see Table S1 for sample size). In three replicates (one from nlow = 18) over a period of 24 h, as described above. In the
each treatment combination except low–low) none of the eggs no-mating treatment, females were paired with a high-condi-
collected emerged as adults, so these replicates were excluded tion or low-condition male (nhigh = 19, nlow = 19) for 24 h,
from analyses of offspring body size. Offspring (ntotal = 1415) but mating was prevented by gluing the male genitalia shut.
were later sexed and photographed in lateral view (after Males were briefly immobilised by cooling, and a drop of
removing wings and legs) using the Leica MS5 stereoscope, medical glue (Leukosan Ultra High Viscosity Cyanoacrylate)
© 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.
1548 A. J. Crean, A. M. Kopps and R. Bonduriansky Letter
was placed over the epandrium to seal the genitalia. Follow- tion) and offspring sex as fixed, categorical effects, and devel-
ing recovery, males behaved normally, but were unable to opment time, maternal body size and second male body size
achieve intromission or sperm transfer (AJC, pers. obs.). All fitted as covariates, along with all two- and three-way interac-
males in this treatment were frozen after 36 h. In the partition tions. This model was re-fitted after eliminating covariates
treatment, females between 1 and 3 weeks of age were housed and interactions that were far from significance (P > 0.2), and
with a high- or low-condition male (nhigh = 19, nlow = 18) on interaction contrasts (Quinn & Keough 2002) were carried out
the opposite side of a mesh partition. At age 3 weeks, females within this model by assigning coefficients (1 or 1) to specific
from all treatments were provided with oviposition media to combinations of treatment levels so as to define and test the
verify that no mating had occurred in the no-mating and par- interactions of interest between first male diet and the levels
tition treatments: as expected, only females in the mating of the housing treatment (mating vs. no-mating; mating vs.
treatment laid fertilised eggs that hatched into larvae. All partition). Female differential allocation based on pre-mating
females were then mated to a new male (all low-condition), assessment would be manifested as an overall (main) effect of
and provided with fresh oviposition medium. From each first male condition. Semen-mediated effects of first male con-
female, 20 eggs were transferred to poor larval medium as dition would be manifested as a first male condition 9 hous-
described above, and adult offspring were counted, sexed and ing treatment interaction, whereby high first male condition
measured as described above (see Table S3 for sample sizes). conferred increased offspring body size only when the first
Approximately 80% of females in this experiment produced male was allowed to mate with the female.
adult offspring for measurement of adult body size (ntotal =
994 adult offspring, Table S3).
RESULTS
Data analysis First and second male condition and offspring phenotype
All data were analysed using JMP (version 10.0.0, SAS Institute We found that the adult body size of offspring was influ-
Inc., Cary, NC, USA). From the telegony experiment, offspring enced positively by the condition of females’ initial mate
body size (thorax length) and egg size (area) were analysed (‘first male’): offspring were ~ 0.5 SD larger when the
using linear mixed models fitted by restricted maximum likeli- female was initially mated to a high-condition male than
hood (REML), with family included as a random effect, first when the female was initially mated to a low-condition
male condition (high or low), second male condition (high or male (Fig 3a). However, offspring body size was not
low) and offspring sex included as fixed, categorical effects, and affected by the condition of females’ subsequent mate (‘sec-
maternal body size, second male body size and development ond male’), or an interaction between first and second
time fitted as covariates. Models were re-fitted after removing
non-significant interactions (always leaving all main effects) Table 1 Effects of first and second male condition (high vs. low) on off-
(Quinn & Keough 2002). To eliminate multicollinearity spring traits (full models including all non-significant interactions are shown
between body size and categorical predictors, male body size in Table S4)
(thorax length) was normalised (mean = 0, SD = 1) within diet Estimate SE d.f. F P
treatment, and offspring body size was normalised within sex.
Egg-to-adult viability was measured as the number of offspring (a) offspring body size
out of 20 eggs that emerged as adults, and developmental time First male condition 0.229 0.090 1 6.491 0.013
Second male condition 0.006 0.088 1 0.004 0.948
was quantified as days between oviposition and first adult emer- Offspring sex 0.014 0.015 1 0.794 0.373
gence. Both variables were analysed using a generalised linear Maternal size 0.213 0.095 1 5.024 0.027
model with Poisson distribution and log link function. Second male size 0.010 0.093 1 0.013 0.911
To verify that first male condition affected offspring sired Developmental time 0.120 0.056 1 4.505 0.037
by the second male, we re-analysed offspring body size using Family (random effect) = 0.700 0.107
only those offspring that showed a genetic match to the sec- (b) egg size
First male condition 0.019 0.070 1 0.074 0.786
ond male. We fitted a linear mixed model as described above,
Second male condition 0.096 0.070 1 1.938 0.167
except that instead of first and second male diet, we tested a Maternal size 0.004 0.002 1 3.723 0.057
treatment effect denoting first and second male’s condition in Family (random effect) = 0.420 0.070
crossover treatments (low–high vs. high–low). We also tested
whether paternity varied with experimental treatment by fit- Estimate SE d.f. v2 P
ting a generalised linear model (Poisson distribution, log link
(c) Offspring egg-to-adult viability
function), with the number of offspring per family sired by
First male condition 0.060 0.035 1 2.924 0.087
the second male as the dependant variable, treatment (high– Second male condition 0.025 0.035 1 0.524 0.470
low or low–high) included as a fixed, categorical effect, and Maternal size 0.149 0.034 1 18.667 <0.001
maternal body size, second male body size and number of
genotyped offspring per family fitted as covariates. Offspring body size (a) and egg size (b) were analysed using linear mixed
models, with replicate (family) included as a random effect. The family
From the differential allocation experiment, offspring body
variance component (proportion of total variance explained SE) is
size was analysed using a linear mixed model fitted by REML, shown below the fixed effects. Offspring egg-to-adult viability (c) was
with family fitted as a random effect, first male condition analysed using a generalised linear model with Poisson distribution and
(high or low), housing treatment (mating, no-mating, parti- log link function. Significant effects are highlighted in bold.
© 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.
Letter Telegonic effects of male condition 1549
(a) (b) Fig. S3). In 35 families (offspring of the same mother) all
genotyped offspring matched the second male, in five families
Condition of
there were no offspring that matched the second male, and in
Normalized offspring body size
0.5
Paternity analysis
As expected, paternity analysis based on microsatellite geno-
typing indicated that a large majority (87%) of offspring were 0.0
sired by the second male (see Supporting Information,
–0.5
Table 2 Analysis of offspring adult body size, based on a reduced data set
including only those offspring that showed a genetic match to the second
male (full model including all non-significant interactions is shown in
Table S4e)
–1.0
Partition No-mating Mating
Estimate SE d.f. F P
Treatment 0.288 0.125 1 5.307 0.027 Figure 4 First male condition effects were mediated by semen rather than
Offspring sex 0.028 0.039 1 0.521 0.472 female differential allocation based on pre-mating assessment of male
Maternal size 0.333 0.126 1 6.970 0.012 quality: first male condition influenced offspring body size when females
Family (random effect) = 0.718 0.178 were mated with the first male, but not when females were able to
interact but not mate with the first male (significant interaction denoted
‘Treatment’ denotes the condition of the first and second male (high-low by connecting lines and asterisk), or when females were separated from
vs. low-high). Effects were estimated in a linear mixed model, with family the first male by a partition. Points show least-squares means SE from
included as a random effect. Significant effects are highlighted in bold. the fitted model (Table S5).
© 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.
1550 A. J. Crean, A. M. Kopps and R. Bonduriansky Letter
© 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.
Letter Telegonic effects of male condition 1551
of offspring sired as much as 2 weeks later by another male, may be able to maximise offspring fitness via mate preferences
that this effect can occur even if the first male fails to achieve that change over the course of the female ontogeny or repro-
any fertilisations, and that such effects can extend to the adult ductive cycle (Richard et al. 2005). For example, females may
phenotype of offspring. benefit by mating with males that optimise semen-dependent
Effects of a female’s previous mate on a subsequent male’s offspring traits while carrying immature ovules, but choosing
offspring could also come about via female differential alloca- males that optimise genetically determined offspring traits fol-
tion of resources to developing oocytes. Theory suggests that lowing ovule maturation (see Fig. 1). Indeed, our results may
females may be selected to assess male quality, and preferen- account for observations of extreme choosiness in immature
tially allocate resources to the progeny of high-quality males females, despite low probability of fertilisation as a result of
(e.g. Burley 1988; Sheldon 2000; Kindsvater et al. 2013). If a strong last-male sperm precedence and/or lack of capacity for
female switches partners, assessment of the previous male long-term sperm storage (Borgia 1981; Jones et al. 1998;
could therefore affect the quantity of resources that a female Bonduriansky & Rowe 2003). Such female behaviour makes
invests in offspring sired by a subsequent male. However, we adaptive sense if male phenotype can influence offspring fitness
found no evidence of differential allocation based on pre-mat- without fertilisation, but not if females can simply ‘trade-up’
ing assessment of male quality in this study: male condition with sequential mate choice (Pitcher et al. 2003).
had positive effects on offspring body size when mating took In summary, we show that adult body size of offspring can
place, but not when females were exposed to males without be influenced by the phenotype of a female’s previous mate
mating. We cannot exclude post-copulatory selection on the rather than the genetic sire in Telostylinus angusticollis. This
basis of chemical cues associated with the ejaculate (i.e. cryptic novel transgenerational effect (an example of telegony)
female choice; see Crean & Bonduriansky 2014). Interestingly, appears to be driven by the condition-dependent influence of
the apparent negative effect of first male condition on off- male seminal fluid on the development of immature ovules.
spring body size in the no-mating treatment group (Fig. 4) The potential for such effects exists in any taxon characterised
suggests that females suffer a cost (manifested in reduced off- by internal fertilisation and polyandry, and such effects could
spring body size) from interacting with high-condition (large) influence the evolution of reproductive strategies.
males but, when mating takes place, this cost is offset by the
positive effect on offspring body size of the semen transferred
by these males. Semen-mediated effects on offspring quality ACKNOWLEDGEMENTS
may thus mitigate the harm to females resulting from pre-mat- We thank Paul Worden from Macquarie University (Sydney,
ing interactions with large males in this species. Australia) and Jackie Chan from the Ramaciotti Centre for
The transgenerational effect we observed has the potential Gene Function Analysis (University of New South Wales,
to play a unique role in evolution because it represents a dis- Sydney, Australia) for running our genetic samples on the
tinct source of variation in fitness. The difference between this ABI 3730, and Margo Adler, Dustin Marshall, Jarrod Had-
source of variation and both genetic inheritance and non- field and four anonymous reviewers for insightful comments
genetic parental effects is analogous to the difference between that greatly improved the manuscript. Funding was provided
vertical and oblique transmission in cultural evolution. by the Australian Research Council through a Discovery
Whereas vertical transmission occurs from parent to offspring, Early Career Researcher Award to AJC and a Discovery
oblique transmission occurs from an unrelated member of the Grant and Future Fellowship to RB.
parental generation, and theoretical studies have shown that
oblique transmission can influence both the dynamics and
equilibria of cultural evolution (e.g. see Cavalli-Sforza & Feld- AUTHORSHIP
man 1981; Findlay et al. 1989; Gong 2010). For analogous
AJC & RB designed the study; AJC performed the research;
reasons, in species lacking culture, oblique transmission (i.e.
AJC & AMK conducted genetic lab work; AJC, AK & RB
telegony) could influence evolutionary trajectories and equilib-
analysed data and wrote the manuscript.
ria – a possibility worth investigating in light of our findings.
Several predictions can be made. Because telegony decouples
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Male diet, female experience, and female size influence maternal
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